Molecular asymmetry of a photosynthetic supercomplex from green sulfur bacteria

Abstract

The photochemical reaction center (RC) features a dimeric architecture for charge separation across the membrane. In green sulfur bacteria (GSB), the trimeric Fenna-Matthews-Olson (FMO) complex mediates the transfer of light energy from the chlorosome antenna complex to the RC. Here we determine the structure of the photosynthetic supercomplex from the GSB Chlorobaculum tepidum using single-particle cryogenic electron microscopy (cryo-EM) and identify the cytochrome c subunit (PscC), two accessory protein subunits (PscE and PscF), a second FMO trimeric complex, and a linker pigment between FMO and the RC core. The protein subunits that are assembled with the symmetric RC core generate an asymmetric photosynthetic supercomplex. One linker bacteriochlorophyll (BChl) is located in one of the two FMO-PscA interfaces, leading to differential efficiencies of the two energy transfer branches. The two FMO trimeric complexes establish two different binding interfaces with the RC cytoplasmic surface, driven by the associated accessory subunits. This structure of the GSB photosynthetic supercomplex provides mechanistic insight into the light excitation energy transfer routes and a possible evolutionary transition intermediate of the bacterial photosynthetic supercomplex from the primitive homodimeric RC.

Structure of the Acidobacteria homodimeric reaction center bound with cytochrome c

“…6a), which was more similar to the distribution of the lowmolecular-weight proteins in PSII 20 (Supplementary Fig. 6e) than to the distribution of surrounding subunits in the HbRC 6 , GsbRC 21,22 and PSI 10 (Supplementary Fig. 6b-d).…”

Experimental and Theoretical Mutation of Exciton States on the Smallest Type-I Photosynthetic Reaction Center Complex of a Green Sulfur Bacterium Chlorobaclum tepidum

“…A small band at approximately 668 nm is attributed to the Q y peaks of four Chl a molecules located adjacent to P840 (with two of them being more distant from P840). According to previous studies, these Chl a molecules serve as electron acceptors A 0 . − , Light illumination at 4 K resulted in a reduction of the peaks at 837 and 668 nm (purple line in Figure ), indicating the photooxidation of P840 (Figure ). The dark minus light (D – L) difference spectrum indicates a positive peak at 837 nm along with a shoulder peak at 825 nm, indicating the bleaching of the P840 Q y peak and the shifts of nearby BChl a ’s and accessory Chl a located adjacent to the special pair P840.…”

“…Figure indicates the absorption spectrum of GsbRC purified from wild-type cells. GsbRC prepared by detergent treatment and His-affinity column chromatography is almost free of FMO, in contrast to the one that binds to one FMO, which is used for structure determination. − The spectrum measured at 4 K in the dark exhibits characteristic Q y BChl a absorption peaks. The spectrum above 700 nm was attributed to antenna BChl a and a special pair of BChl a and BChl a ′ dimers (P840).…”

“…These different yet highly efficient solar energy conversion systems have evolved and adapted to diverse light conditions and environments. We performed theoretical and mutational analyses of a green sulfur bacterium Chlorobaculum tepidum type-I RC (GsbRC) pigment system − whose structure was recently identified using cryo-electron microscopy (cryo-EM) as a type-I RC with the lowest number of pigments.…”

Cryo‐electron microscopy structure of the intact photosynthetic light‐harvesting antenna‐reaction center complex from a green sulfur bacterium

“…During the preparation and revision of this manuscript, Puskar et al (2022) reported a similar structure of the GsbRC‐2FMO supercomplex purified from the same organism at a similar resolution. The overall structure of this GsbRC‐2FMO supercomplex is very similar to that in our present study and both structures contain a second FMO trimer, two novel subunits (PscE and PscF) and a linker pigment (BChl‐816) at the interface between first FMO trimer and the GsbRC core.…”